Cross talk between the sporophyte and the megagametophyte during ovule development

Abstract

In seed plant ovules, the diploid maternal sporophytic generation embeds and sustains the haploid generation (the female gametophyte); thus, two independent generations coexist in a single organ. Many independent studies on Arabidopsis ovule mutants suggest that embryo sac development requires highly synchronized morphogenesis of the maternal sporophyte surrounding the gametophyte, since megagametogenesis is severely perturbed in most of the known sporophytic ovule development mutants. Which are the messenger molecules involved in the haploid-diploid dialogue? And furthermore, is this one way communication or is a feedback cross talk? In this review, we discuss genetic and molecular evidences supporting the presence of a cross talk between the two generations, starting from the first studies regarding ovule development and ending to the recently sporophytic identified genes whose expression is strictly controlled by the haploid gametophytic generation. We will mainly focus on Arabidopsis studies since it is the species more widely studied for this aspect. Furthermore, possible candidate molecules involved in the diploid-haploid generations dialogue will be presented and discussed.

Cytochrome P450CYP78A9Is Involved in Arabidopsis Reproductive Development

“…The gametophytic mutants characterized until now all have normal development of sporophytic tissues. Accordingly, a hierarchical communication between the two generations has been suggested, assigning a higher order to the sporophytic maternal tissues (Bencivenga et al, 2011). The fruit without fertilization (fwf/arf8) Arabidopsis parthenocarpic The values shown are averages of the relative peak response area in three replicates 6 SE.…”

“…Nevertheless, which class of messengers are involved (e.g. metabolites, small peptides, or hormones) has not been deciphered yet (Vivian-Smith et al, 2001;Bencivenga et al, 2011;Mizzotti et al, 2012). Previous work using cyp78a mutants and CYP78A-overexpressing plants proposed that CYP78A family members are involved in the generation of novel signaling compounds that are mainly related to the control of organ size and shape as well as plant architecture (Ito and Meyerowitz, 2000;Miyoshi et al, 2004;Anastasiou et al, 2007;Adamski et al, 2009).…”

Cross-Talk Between Sporophyte and Gametophyte Generations Is Promoted by CHD3 Chromatin Remodelers inArabidopsis thaliana

“…The female gametophyte develops within the sporophytic ovary, where it forms into an embryo sac as it is surrounded by the diploid sporophytic integuments of the ovule (Bencivenga et al 2011;Chevalier et al 2011). Characterization of ovule-defective mutants in Arabidopsis thaliana has revealed that female gametophyte development is dependent on the sporophyte, particularly integument development, and has also identified a variety of factors that contribute to this relationship including transcription factors, kinases, and components of plant hormone signal transduction pathways (Bencivenga et al 2011;Shi and Yang 2011;Vielle-Calzada et al 2012). Some of these factors are expressed uniquely in the integuments, whereas others are more widely expressed.…”

“…However, it does not explain the defect in integument development observed in pkl plants prior to pollination (Figure 3). We therefore tested whether loss of PKL results in altered expression of genes that contribute to development of the integuments (Bencivenga et al 2011). Mature pistils were harvested immediately prior to anther dehiscence, and expression levels of several genes involved in ovule development were analyzed using qRT-PCR.…”

“…Given the nature of each defect (reduced, but not absent, rate of pollen tube growth as opposed to abortion of embryo sacs), we hypothesize that the defect in pollen tube growth leads to delayed asynchronous fertilization and ensuing delayed asynchronous embryo development, whereas failed ovule development leads to reduced seed set. In the absence of the ability to uncouple the pollen tube defect from the ovule defect, however, it is possible that the observed ovule defects contribute to the delay in embryogenesis and/or that the pollen tube defects contribute to reduced seed set.There is strong precedent for control of pollen tube development or embryo sac development by factors in the maternal sporophytic tissues (Bencivenga et al 2011;Dresselhaus and Franklin-Tong 2013;Leydon et al 2014). PKL is unusual, however, in that it contributes to both processes.…”